SWARMING ACTIVITY OF BATS AT THE ENTRANCE OF LILIECILOR CAVE FROM RARĂU MOUNTAINS

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1 Analele Științifice ale Universității Alexandru Ioan Cuza din Iași, s. Biologie animală, Tom LVIII, 2012 SWARMING ACTIVITY OF BATS AT THE ENTRANCE OF LILIECILOR CAVE FROM RARĂU MOUNTAINS Irina POCORA, Viorel POCORA and Emanuel Ștefan BALTAG Al. I. Cuza University Iași, Faculty of Biology, Bd. Carol I 20A, Iași, Romania, irinaif23@yahoo.com Abstract: Swarming activity of bats at underground hibernacula, during late summer and autumn, has been poorly investigated in the eastern part of Europe. The bat activity at the cave entrance has the pick in the swarming period which starts at the beginning of August until the middle of October. During this period we investigate the bats species from Liliecilor Cave, Rarău Mountains using mist nets and ultrasound detectors. Among all 9 swarming species captured, Myotis myotis and Myotis oxygnathus were the dominant ones (79%). Sex ratio is different from other swarming reported studies for Myotis myotis, being the only species in which females prevail in captures. Keywords: bats, autumn swarming, Myotis myotis, Myotis oxygnathus. Rezumat: Activitatea de împerechere a liliecilor la intrarea în Peștera Liliecilor din Rarău. Activitatea de împerechere a liliecilor, vara târziu și toamna, la intrarea în adăposturile cavernicole de hibernare, a fost puțin investigată în estul Europei. Vârful activității liliecilor de la intrarea în peșteră are loc de la începtulul lunii august până la mijlocul lunii octombrie. În această perioadă, cu ajutorul plaselor chiropterologice și a detectorului de ultrasunete, am investigat speciile de lilieci de la Peștera Liliecilor din Rarău. Dintre cele 9 specii de lilieci capturate în perioada de împerechere, Myotis myotis și Myotis oxygnathus au fost speciile dominante (79%). Față de alte studii, sex ratio este diferit pentru specia Myotis myotis, fiind singura specie la care au predominat femelele în capturi. Cuvinte cheie: lilieci, împerechere de toamnă, Myotis myotis, Myotis oxygnathus. Introduction The first observations during autumn, concerning a large number of bats that visit the caves and mines few months before hibernation, were first described in North America, in the 60 s (Fenton, 1969). This type of behaviour is called autumn swarming (Fenton, 1969). Swarming involves bats chasing each other at the entrance of the cave and emitting various social calls, many times without remaining in the cave during the day (Fenton, 1969; Parsons et al., 2003a; Rivers et al., 2006). Up to many hundreds of bats may arrive and depart during one night in one shelter (Parsons et al., 2003b). Such an intensive visitations of caves, during the migratory periods, was described also in Central Europe as swarming behaviour of bats (Pandurska & Beshkov, 1998). It has been suggested that the swarming is a mating event that facilitates the change of genes between the bats from isolated summer colonies, assessing hibernacula and show the location of hibernacula to offspring (Kerth et al., 2003; Rivers et al., 2005). Even if the majority of bat studies from Romania were conducted in caves, only one study refers to the mating activity at the entrance of an underground shelter (Jére et al., 2007). The aim of this study is to describe the species richness during late summer and autumn period and to prove that Liliecilor Cave from Rarău Mountain is used as a swarming shelter by the bats

2 Irina Pocora et al. Material and Methods Liliecilor Cave is situated in Rarău Mountains (Suceava County, N, E, 1492 m. a. s. l.). This cave is a scientific protected area and it covers an area of 6 hectares. The surroundings habitat is represented by coniferous forest. During we visited Liliecilor Cave five times, to study the bats activity in this period of the year. Mist nets were placed at the cave entrance in 7 nights from August 2005 ( and ), one night in July (2006), one night in October 2007 (04.10) and one night in September 2008 (02.09). The capturing rate had the lowest level during July (2006), with 0 bats/trap/night and the highest, of 52 bats/trap/night on The mist nets were anchored after sunset until 2 AM. Using mist nets we trapped 183 bats from 9 species: Myotis myotis, Myotis oxygnathus, Myotis daubentonii, Myotis mystacinus, Myotis bechsteinii, Myotis nattereri, Myotis brandtii, Plecotus auritus and Eptesicus nilssonii. With the help of the heterodyne detector there was also signaled Rhinolophus hipposideros species (in May and September), and based on the recordings with the time expansion detector, we observed that in September, the entrance of the cave was also transited by Pipistrellus pygmaeus ( ). For bats trapping we used mist nets of 7 and 12 m length and 2.5 high. Bats were measured with the calliper (±0.5 mm), weighed with Pesola scale of 60g (±0.5 g) from Ecotone, the teeth were observed with a magnifier glass of 10x. For the identification of the bats we also used ultrasound detectors: heterodyne (Batbox Duet) and time expansion (Tranquility). The species were identified with the help of identification keys (Schober & Grimmberger, 1996; Dietz & Helversen, 2004). Results and Discussion The dominant species during trapping were the sibling species: Myotis myotis (46.4%) and Myotis oxygnathus (32.2%) (Fig. 1), these also being characteristic species for the shelter, in the hibernation period. Concerning the other bat species: Plecotus auritus (4.2%), Myotis nattereri (2.8%) and Myotis brandtii (3.1%) are accessory species, and Myotis mystacinus, Myotis daubentonii, Myotis bechsteinii and Eptesicus nilssonii are accidental species, with less than 1% (Table 1). Figure 1. The percent of bat species captured in the mist nets in Liliecilor Cave - Rarău Mountain

3 Analele Științifice ale Universității Alexandru Ioan Cuza din Iași, s. Biologie animală, Tom LVIII, 2012 Regarding the proportion of females versus males, the value tilt to females (1.5) only for Myotis myotis (Fig. 2). For the other species of bats trapped in mist nets, the majority were males, except for Myotis mystacinus for which we record a sex ratio of 1:1. Outside of the hibernation season (June) in Liliecilor Cave from Rarău Mountains we counted a maximum of 30 individuals of Myotis oxygnathus/myotis myotis (Table 1). Using ultrasound detector in this period we identify also other species: Rhinolophus hipposideros, Myotis mystacinus/myotis brandtii, Myotis nattereri, Myotis daubentonii, Plecotus auritus/plecotus austriacus. In the first two weeks of July, there were no bats captured with the mist net. The bats come for mating, at the end of July and until they enter in hibernation. Table 1. The ecological indices: dominance (D), constancy (C) and the ecological signification value (W) for bat species trapped in the mist nets during mating period (No. ind. Number of individuals). Species No. ind. Dominance Constancy W % % % Myotis myotis D5 100 C W5 Myotis oxygnathus D5 100 C W5 Plecotus auritus 11 6 D C3 4.3 W3 Myotis nattereri D C3 2.8 W3 Myotis brandtii D C3 3.1 W3 Myotis mystacinus D C1 0.3 W2 Myotis daubentonii D C2 0.6 W2 Eptesicus nilssonii D C2 0.3 W2 Myotis bechsteinii D C W1 Figure 2. The sex ratio for 7 species of bats captured in mist nets at Bats Cave from Rarău Mountains (August-October 2005, 2007, 2008), shown in the number of females versus the number of males

4 Irina Pocora et al. Chachula et al. (2008) mention that on 22 nd of July 2003, within the program of Monitoring of subterranean habitats concerning the bats from Romania, there were captured 29 bats in the mist nets: 14 Myotis oxygnathus, 10 Myotis myotis, 1 Myotis daubentonii, 2 Myotis dasycneme, 1 Myotis mystacinus, and 1 Myotis brandtii. The identifications were made by Tomasz Postawa and Anna Gas. Tomasz Postawa has observed a nursing colony of 70 exemplars of bats in the cave, but the affirmation is not confirmed, because Nagy and Postawa (2010) do not mention this in their paper. Considering that the cave is cold and the altitude is high, it cannot shelter a nursing colony of Myotis oxygnathus/myotis myotis. Our hypothesis is sustained also by the observation from 1 st of June 2007, when in the cave there were observed only solitary individuals, which were hibernating. During the reproduction period, the Myotis oxygnathus/myotis myotis species descend to lower altitudes, under 1000 meters (Drescher, 2004), and the nursing colony of this species needs higher temperatures, of around 30ºC (Valenciuc, 1971; Benda et al., 2003). Furthermore, in the previous studies, in June and July there were not identified any bats in the cave (Valenciuc, 1989). Parsons et al. (2003a) mention that, at the entrance of the caves, bat trapping during spring and early summer months show a low usage. Many bats are flying at the entrance of Liliecilor Cave from Rarău Mountains, from the end of July. In the autumn, the increase of trapped bat species is connected with seasonal migrations and the choice of winter quarters (Pandurska & Beshkov, 1998). In this study, swarming behaviour was recorded for nine bat species, which all usually hibernate in underground sites (Pocora et al., 2008). This supports the general opinion that autumn swarming behaviour is characteristic to those bat species using underground sites for hibernation (Parsons et al., 2003a). The most intense activity, in the mating period, was observed at the caves with vertical entrance (Glover & Altringham, 2008). The same authors have observed that it is not a significant relation between the activity of bats and altitude. The species that were captured at Liliecilor Cave from Rarău Mountains belonged, in majority, to Myotis genus, fact observed also in the majority of swarming studies from Europe and North America (Parsons et al., 2003a). At Liliecilor Cave from Rarău Mountain, during mating period, the dominant species are the ones that hibernate here (Myotis myotis 46.4% and Myotis oxygnathus 32.2%). In some caves from Vârghiș Gorge, were also trapped mainly the sibling species Myotis myotis/myotis oxygnathus (Jére et al., 2007). Most of the individuals that were trapped were caught entering in the hibernacula, and they are mating before entering in hibernation. The other species that were captured represented only 21% of the captures. Probably the reason for which the other species use the cave for hibernation in small amount is the high altitude. These species are using hollows as shelter during summer and usually they occur at low altitudes. Bats do not exclusively hibernate at the sites were they swarm (Parsons et al., 2003a). In other studies from Europe, the species that dominated were other species of Myotis and not the sibling species Myotis myotis and Myotis oxygnathus (Parsons et al., 2003a; Rivers et al., 2006; Šuba et al., 2008; Glover & Altringham, 2008). In Europe there are not any studies on the swarming behaviour of the sibling species Myotis myotis and Myotis oxygnathus. The only study, regarding the mating of Myotis myotis from buildings is from Zahn and Dippel (1997) and the authors specify that the mating takes place from August to October. Zahn and Dippel (1997) assuming that most of the mating activity

5 Analele Științifice ale Universității Alexandru Ioan Cuza din Iași, s. Biologie animală, Tom LVIII, 2012 occurs at male roost sites (in buildings). Based on their observations they show that mating occur accidental in hibernating sites. From studies on Myotis myotis at caves from Bavaria, males were observed only in a few cases of mating during September and October. In these studies there was suggested that the main mating season ends before the bats appear at the caves in large numbers. We observed that the swarming season at Liliecilor Cave from Rarău Mountain takes place from the beginning of August to the half of October. Possibly also in November, when there is still activity at the cave entrance (Valenciuc & Ion, 1965) and the temperature are still high. In the first study from Liliecilor Cave, Rarau Mountain, the authors believed that the bats, that were initially sheltering in less favourable places because of the climatic conditions, woke up to search for a better place. More intensive activity of swarming species, at Liliecilor Cave, was observed at the entrance during the end of August and in the beginning of September. The lowest rate of capturing was in October (6.3 bats per hour) and at the beginning of August (7.5 bats/hour), and the highest rate was at the end of August (15.3 bats/h) and at the beginning of September (13 bats/hour). Autumn swarming season in UK take place from mid-august to mid-november, peaking from mid-september to mid-october (Rivers et al., 2006; Glover & Altringham, 2008). In Latvia, the greatest swarming activity for most species was observed at the end of August and in September (Šuba et al., 2008). Valenciuc & Ion (1969a) specify that the highest activity at the entrance of the cave was in September. They observed that there are bats that visit the cave during night time, without staying during the day. Also, they observed that the entrance is transited by more bat species, but without proper equipment they could not specify what species those were. The sex-ratio was found to be biased towards males in all species, as observed in most swarming studies (Rivers et al., 2006), with two exception for Myotis myotis, in which case the females dominated, and Myotis mystacinus for which we record a sex ratio of 1:1. Valenciuc and Ion (1965), based on the captures made from August to November, specify that at the sibling species Myotis myotis/myotis oxygnathus, the males are in a larger number than the females (59% males over 42% females). The high male number which was found at all sites for the Myotis species may be due to the more nomadic behaviour of males which are visiting swarming sites more often than females during the swarming season while, females are more faithful to a home range, before requiring an underground hibernacula during harsh weather (Parsons et al., 2003a). Males have more to gain from maximizing the number of mating than females and should therefore visit swarming sites more often and stay longer, consistent with the finding that recapture rates are higher amongst males than females (Rivers et al., 2006). The males of Myotis myotis and Myotis oxygnathus, trapped in Liliecilor Cave from Rarau Mountains were presenting sexual characteristics during mating period. Considering that and the fact that the main percent of the trapped individuals were males, and the bats were chasing each other, we conclude that Liliecilor Cave from Rarău Mountain is an important site for swarming species, especially for this two sibling s species. Also, using the time expansion detector we gather social calls (Fig. 3), emitted in September, from swarming bats. This type of ultrasounds was described also by Pfalzer (2002) in other swarming sites

6 Irina Pocora et al. Figure 3. Myotis myotis/m. oxygnathus social calls, Liliecilor Cave from Rarău Mountains, The result of this study support the hypothesis, were emitted for another species (Šuba et al., 2008; Glover & Altringham, 2008), that biological function of swarming behaviour for Myotis myotis/myotis oxygnathus is related with hibernacula assessment or information transfer by means of showing the location of hibernacula to the other individuals. This study has conservation significance for monitoring, and for describing the distribution of bat species. Protection. Nagy and Postawa (2010), evaluated the degree of conservation of the underground shelters from Romania, based on the observations from 2003, they gave level 2 of conservation for Liliecilor Cave from Rarău Mountain (conservation value between 1 to 4, 1 is the highest and 4 the lowest). From the 31 species which were recorded in Romania (Nagy & Postawa, 2010), at Liliecilor Cave from Rarău Mountain, were identified 11 species. Four of these species: Myotis myotis, Myotis oxygnathus, Myotis bechsteinii, Rhinolophus hipposideros are included in Appendix II of the Habitat Directive (92/43 EEC). The identification of swarming sites has recently been recognized as an important element in propose of the pan-european monitoring scheme. Clearly, swarming sites will have a special consideration in conservation management strategies for cave-dwelling bats (Parsons et al., 2003a). Old custodians of Liliecilor Cave from Rarău Mountains wanted to close this cave with metal bars, but the cave is naturally protected, the entrance being represented by an abyss of 14 m, followed by a crack in the bottom rock of 7 m depth, in which, during winter, the access is more difficult. Blocking of entrance to bat hibernacula can change the microclimate of the cave, but also the species compositions and/or abundance of hibernating bats. If the entrances of underground hibernation sites of bats are being planned to close against humans and predators like cats and martens, these actions should not make the microclimate unsuitable for bats (Baranauskas, 2006). Even quite small changes to the

7 Analele Științifice ale Universității Alexandru Ioan Cuza din Iași, s. Biologie animală, Tom LVIII, 2012 topography of a site, both inside and outside, can have far reaching effects on its suitability for bats, mainly by altering the air-flow through the system and hence the temperature and humidity (Mitchell-Jones et al., 2000). The consequences of gates to swarming behaviour and long-term use of the site by bats are unknown (Pugh & Altringham, 2005). Conclusions In this study, swarming behaviour was recorded for nine bat species, which all usually hibernate in underground sites: Myotis myotis, Myotis oxygnathus, Myotis daubentonii, Myotis mystacinus, Myotis bechsteinii, Myotis nattereri, Myotis brandtii, Plecotus auritus and Eptesicus nilssonii. At Liliecilor Cave from Rarău Mountain, during mating period, the dominant species are the ones that hibernate here (Myotis myotis 46.4% and Myotis oxygnathus 32.2%). We observed that the swarming season at Liliecilor Cave from Rarău Mountain takes place from the beginning of August to the half of October. More intensive activity of swarming species, at Liliecilor Cave, was observed at the entrance during the end of August and in the beginning of September. Acknowledgements This work was possible through the project CNCSIS PD 326/2010, funded by the Romanian Education and Research Office for I. Pocora, POSDRU/89/1.5/S/49944/2010, for V. Pocora and by the European Social Fund in Romania, under the responsibility of the AMPOSDRU [grants POSDRU/CPP 107/DMI 1.5/S/78342] for E. Baltag. The authors are grateful to Farkas and Abigel Szodoray-Paradi from APLR (Bat Association from Romania), Adrian and Tatiana Done (Speo Bucovina Foundation) for the equipment, funding and the support given. Thank you to all field assistants: Loredana Asoltani, Mihaela Ionescu, Daniel Busuioc, Lucian Fusu, Ionut Iorgu, Simona Asoltani, Daniela Cuzic. References Baranauskas, K., Bat species composition and abundance in two undergrounds hibernacula in Vilnius before and after fencing. Ekologija, 1: Benda, P., Ivanova, T., Horacek, V., Cerveny, J., Gaisler, J., Gueorguieva, A., Petrov, B., Vohralik, V., Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 3. Review of bat distribution in Bulgaria. Acta Soc. Zool. Bohem., 67: Chachula, O., Valenciuc, N., Done, A., Contributions to the study of Chiroptera from Moldavia (Romania). Anal. Știin. Univ. Al I. Cuza, Iași, s. Biol. animala, 54: Dietz, C., Helversen, O. V., Ilustrated identification key to the bats of Europe. Tuebingen and Erlangen (Germany). Drescher, C., Radiotracking of Myotis myotis (Chiroptera: Vespertilionidae) in South Tyrol and implications for its conservation. Mammalia, 68 (4): Fenton, M. B., Summer activity of Myotis lucifugus (Chiroptera: Vespertilionidae) at hibernacula in Ontario and Quebec. Can. J. Zool., 47: Glover, A. M., Altringham J. D., Cave selection and use by swarming bat species. Biological Conservation, 141: Jére, C., Doóczy, A., Barti, L., Results of research on the bat fauna of the Vârghiș Gorge (Eastern Carpathians, Romania). Trav. Inst. Spéol. Émile Racovitza, 45-46: Kerth, G., Kiefer, A., Trappmann, C., Weishaar, M., High gene diversity at swarming sites suggests hot spots for gene flow in the endangered Bechstein s bat. Cons. Genet. 4:

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